[Federal Register: November 19, 2007 (Volume 72, Number 222)]
[Rules and Regulations]
[Page 65171-65204]
From the Federal Register Online via GPO Access [wais.access.gpo.gov]
[DOCID:fr19no07-12]
[[Page 65171]]
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Part III
Department of Agriculture
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Animal and Plant Health Inspection Service
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7 CFR Parts 301 and 305
Citrus Canker; Movement of Fruit From Quarantined Areas; Final Rule
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DEPARTMENT OF AGRICULTURE
Animal and Plant Health Inspection Service
7 CFR Parts 301 and 305
[Docket No. APHIS-2007-0022]
RIN 0579-AC34
Citrus Canker; Movement of Fruit From Quarantined Areas
AGENCY: Animal and Plant Health Inspection Service, USDA.
ACTION: Final rule.
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SUMMARY: We are amending the citrus canker regulations to modify the
conditions under which fruit may be moved interstate from a quarantined
area. We are eliminating the requirement that the groves in which the
fruit is produced be inspected and found free of citrus canker, and
instead are requiring that every lot of fruit produced in the
quarantined area be inspected by the Animal and Plant Health Inspection
Service at a packinghouse operating under a compliance agreement and
found to be free of visible symptoms of citrus canker. We are retaining
the requirement that the fruit be treated with a surface disinfectant
and the prohibition on the movement of fruit from a quarantined area
into commercial citrus-producing States. These changes will relieve
some restrictions on the interstate movement of fresh citrus fruit from
Florida while maintaining conditions that will help prevent the
artificial spread of citrus canker.
DATES: Effective Date: November 19, 2007.
FOR FURTHER INFORMATION CONTACT: Mr. Stephen Poe, Senior Operations
Officer, Emergency and Domestic Programs, Plant Protection and
Quarantine, APHIS, 4700 River Road Unit 137, Riverdale, MD 20737-1231;
(301) 734-4387.
SUPPLEMENTARY INFORMATION:
Background
Citrus canker is a plant disease caused by the bacterium
Xanthomonas axonopodis pv. citri (referred to below as Xac) that
affects plants and plant parts, including fresh fruit, of citrus and
citrus relatives (Family Rutaceae). Citrus canker can cause defoliation
and other serious damage to the leaves and twigs of susceptible plants.
It can also cause lesions on the fruit of infected plants, which render
the fruit unmarketable, and cause infected fruit to drop from the trees
before reaching maturity. The aggressive A (Asiatic) strain of citrus
canker can infect susceptible plants rapidly and lead to extensive
economic losses in commercial citrus-producing areas. Citrus canker is
only known to be present in the United States in the State of Florida.
The regulations to prevent the interstate spread of citrus canker
are contained in Sec. Sec. 301.75-1 through 301.75-14 of ``Subpart--
Citrus Canker'' (7 CFR 301.75-1 through 301.75-17, referred to below as
the regulations). The regulations restrict the interstate movement of
regulated articles from and through areas quarantined because of citrus
canker and provide, among other things, conditions under which
regulated fruit may be moved into, through, and from quarantined areas
for packing. These regulations are promulgated pursuant to the Plant
Protection Act (7 U.S.C. 7701 et seq.).
On June 21, 2007, we published in the Federal Register (72 FR
34180-34191, Docket No. APHIS-2007-0022) a proposal \1\ to amend the
citrus canker regulations by modifying the conditions under which fruit
may be moved interstate from quarantined areas. We proposed to
eliminate the requirement that the groves in which the fruit is
produced be inspected and found free of citrus canker, and instead
proposed to require that every lot of fruit produced in the quarantined
area be inspected by the Animal and Plant Health Inspection Service
(APHIS) at a packinghouse operating under a compliance agreement and
found to be free of visible symptoms of citrus canker. We proposed to
retain the requirement that the fruit be treated with a surface
disinfectant and the prohibition on the movement of fruit from a
quarantined area into commercial citrus-producing States.
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\1\ To view the proposed rule, the supporting analyses, and the
comments we received, go to http://www.regulations.gov/fdmspublic/
component/main?main=DocketDetail&d=APHIS-2007-0022.
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We solicited comments concerning our proposal for 30 days ending
July 23, 2007. We subsequently reopened and extended the deadline for
comments until August 7, 2007, in a document published in the Federal
Register on July 27, 2007 (Docket No. APHIS-2007-0022, 72 FR 41239). We
received 72 comments by the close of the comment period. They were from
producers, exporters, researchers, and representatives of State
governments. They are discussed below by topic.
Pest Risk Assessment and Risk Management Analysis
To inform the deliberations that led to the proposed rule, we
prepared two documents that addressed the risk associated with the
interstate movement of citrus fruit from a quarantined area: A pest
risk assessment (PRA) and a risk management analysis (RMA). The PRA,
which was titled ``Evaluation of asymptomatic citrus fruit (Citrus
spp.) as a pathway for the introduction of citrus canker disease
(Xanthomonas axonopodis pv. citri),'' considered all available evidence
associated with asymptomatic citrus fruit as a pathway for the
introduction of citrus canker. The PRA concluded that asymptomatic,
commercially produced citrus fruit treated with a surface disinfectant
and subject to other mitigations is not epidemiologically significant
\2\ as a pathway for the introduction and spread of citrus canker. We
first made this document available for comment on April 6, 2006, when
we published a notice in the Federal Register (71 FR 17434-17435,
Docket No. APHIS-2006-0045), announcing its availability for comment
for 60 days; the comment period was subsequently extended to 90 days.
We also submitted it for peer review in accordance with the U.S.
Department of Agriculture (USDA) guidelines for peer review developed
in response to the Office of Management and Budget's peer review
bulletin. We received 19 comments by the end of the comment period,
which we also submitted to the peer review panel members for their
consideration.\3\ We carefully considered the comments of the public
and peer reviewers, and made revisions to the analysis based on
concerns they raised. The revisions did not change the conclusions of
the PRA; the revised version of the PRA was provided with the proposed
rule.
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\2\ We use the term ``epidemiologically significant'' to refer
to minimum conditions required for disease transmission.
\3\ The original PRA and the comments we received on it can be
viewed at http://www.regulations.gov/fdmspublic/component/
main?main=DocketDetail&d=APHIS-2006-0045.
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In light of the comments by the public and peer reviewers, it
became clear that additional analysis was necessary to apply the
conclusions of the PRA to the situation in Florida. In order to apply
the conclusions of the PRA, we needed to extend its application to
evaluate methods by which fruit \4\ could be produced, treated,
inspected, packaged, and shipped without resulting in the
[[Page 65173]]
spread of citrus canker to commercial citrus-producing areas.
(Commercial citrus-producing areas are listed in Sec. 301.75-5 of the
regulations and are referred to in this document as commercial citrus-
producing States. Those States, listed in Sec. 301.75-5(a), are:
American Samoa, Arizona, California, Florida, Guam, Hawaii, Louisiana,
Northern Mariana Islands, Puerto Rico, Texas, and the U.S. Virgin
Islands.)
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\4\ Given the practical difficulties in ensuring that only
asymptomatic fruit enters interstate commerce under any regulatory
strategy, we refer here to host fruit in general.
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To address the considerations described above, APHIS prepared the
RMA, which was titled ``Movement of commercially packed fresh citrus
fruit (Citrus spp.) from citrus canker (Xanthomonas axonopodis pv.
citri) disease quarantine areas, March 2007.'' We made the RMA
available for comment along with the proposed rule.\5\ The RMA was also
submitted for peer review, which occurred concurrently with the public
comment period for the proposed rule.\6\ The RMA analyzed the potential
of fresh commercially packed citrus fruit and associated packing
material to serve as a pathway for the introduction and spread of
citrus canker into new areas. It also identified and evaluated options
for regulating the interstate movement of citrus fruit from quarantined
areas with the goal of reducing the potential for citrus canker
introduction and spread. The recommendations in the RMA served as the
basis for the proposed rule.
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\5\ The RMA is available on the Regulations.gov Web site and in
our reading room (see ADDRESSES above) and may be obtained from the
person listed under FOR FURTHER INFORMATION CONTACT.
\6\ The peer review materials for the RMA may be viewed at
http://www.aphis.usda.gov/peer--review/peer--review--agenda.shtml.
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To develop the RMA, we reviewed available evidence regarding the
biology and epidemiology of Xac and the management of citrus canker
disease. The RMA concluded that the introduction and spread of Xac into
other commercial citrus-producing States through the movement of
commercially packed fresh citrus fruit from quarantined areas is
unlikely because:
Fresh citrus fruit is produced and harvested using
techniques that reduce the prevalence of Xac-infected fruit;
Citrus fruit is commercially packed using techniques that
reduce the prevalence of infected or contaminated fruit, including
disinfectant treatment for epiphytic contamination;
For a successful Xac infection that results in disease
outbreaks to occur, an unlikely sequence of events would have to occur;
Reports of citrus canker disease outbreaks linked to fresh
fruit are absent; and
Large quantities of fresh citrus fruit shipped from
regions with Xac have not resulted in any known outbreaks of citrus
canker disease.
Nevertheless, the RMA concluded that the evidence is not currently
sufficient to support a determination that fresh citrus fruit produced
in a Xac-infested grove cannot serve as a pathway for the introduction
of Xac into new areas. Therefore, the RMA evaluated several
packinghouse-centered risk management options for the interstate
movement of fresh commercially packed citrus fruit from regions
infested with citrus canker to regions without the disease. These
packinghouse-centered risk management options were evaluated to
determine whether they provide an appropriate level of phytosanitary
protection without the resource constraints and other practical
considerations that make it difficult to maintain the grove-centered
regulatory approach in Florida. The risk management options evaluated
were:
Option 1: Allow unrestricted distribution of all types and
varieties of commercially packed citrus fruit to all U.S. States.
Option 2: Allow distribution of all types and varieties of
commercially packed citrus fruit to all U.S. States, subject to
packinghouse treatment with APHIS-approved disinfectant and APHIS
inspection of finished fruit that has completed the packinghouse
culling, washing, disinfection, and grading processes.
Option 3: Allow distribution of all types and varieties of
commercially packed citrus fruit (except tangerines) in U.S. States
except commercial citrus-producing States. Allow distribution of
commercially packed tangerines to all U.S. States, including commercial
citrus-producing States. Require packinghouse treatment of all such
citrus fruit with APHIS-approved disinfectant and APHIS inspection of
finished fruit (all types and varieties) for citrus canker disease
symptoms.
Option 4: Allow distribution of all types and varieties of
commercially packed citrus fruit in U.S. States except commercial
citrus-producing States and require packinghouse treatment of citrus
fruit with APHIS-approved disinfectant and APHIS inspection of finished
fruit (all types and varieties) for citrus canker disease symptoms.
Option 5: Leave the current regulations for the interstate
movement of citrus fruit from citrus canker quarantined areas in place
and unchanged.
We proposed to implement Option 4. This option would have limited
distribution of all types and varieties of citrus fruit to States other
than commercial citrus-producing States, with mitigations conducted at
packinghouses operating under compliance agreements. Those mitigations
are the use of an approved disinfectant for all fruit and APHIS
phytosanitary inspection.
We received several comments on the overall level of risk
associated with the movement of commercially packed citrus from a
citrus canker quarantined area, as well as our selection of Option 4.
These comments have not led us to change our determination that Option
4 is the most appropriate option to implement. The RMA that we are
making available with this final rule contains revisions based on the
comments we received on the proposed rule and the comments we received
through the peer review process, but its overall conclusion is the
same. Accordingly, this final rule implements Option 4. (We are making
some changes to the regulatory requirements associated with the
implementation of Option 4. These changes are discussed later in this
document.)
Some commenters believed that the evidence presented in the RMA
warranted the selection of Option 2, which would have allowed the
distribution of citrus fruit to all States, subject to packinghouse
treatment with APHIS-approved disinfectant and APHIS inspection of
finished fruit. These commenters stated that it was extremely unlikely
that the circumstances necessary for the movement of commercially
packed fresh citrus fruit to result in the introduction and spread of
Xac into other commercial citrus-producing States would ever occur.
One commenter stated that the decision to allow the movement of
regulated fruit from a citrus canker quarantined area only into States
other than commercial citrus-producing States, rather than into all
States, was based on politics rather than on science.
One commenter stated that no Florida citrus fruit infected with
citrus canker has ever been found in a commercial citrus-producing
State under the current regulations and that, at the commenter's
packinghouse, not a single piece of fruit with citrus canker had been
found by any inspectors or employees during the last growing season.
One commenter noted more generally that citrus canker has not been
found outside Florida since the disease was first detected there, and
stated that more certainty than uncertainty exists regarding the risk
of commercially
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packed citrus fruit as a viable pathway for citrus canker.
Another commenter noted that the PRA stated the following in its
executive summary: ``The combination of conditions necessary for
introduction are so difficult to achieve that the likelihood of such
occurrence is greater than the baseline exposure represented by
unregulated pathways. The conclusions of the evaluation are reinforced
by a strong record of empirical data from experience and
interceptions.''
We acknowledge the efforts of the Florida citrus industry to put
safeguards in place against citrus canker infestation. The proposed
rule recognized the effectiveness of those safeguards by providing for
the interstate movement to States other than commercial citrus-
producing States of any lot of citrus fruit that is commercially
packed, treated with APHIS-approved disinfectant, and inspected by
APHIS and found to be free of visible canker lesions.
The RMA concludes that commercially packed fresh citrus fruit is an
unlikely pathway for the introduction and spread of Xac and that a
phytosanitary inspection ensures, with high confidence, that few
shipped fruit would have symptoms of citrus canker disease. However,
the model in Appendix 1 to the RMA indicates the potential for some
commercially packed fruit with visible canker lesions to be shipped to
commercial citrus-producing States. That potential for such fruit to
reach commercial citrus-producing States, coupled with the
aforementioned uncertainty regarding fruit as a pathway, led to the
determination that the additional mitigation of prohibiting
distribution to commercial citrus-producing States was required. If, in
the future, evidence is developed to support a determination that
commercially packed citrus fruit (both symptomatic and asymptomatic) is
not an epidemiologically significant pathway for the introduction and
spread of citrus canker, we would undertake rulemaking to amend our
regulations accordingly.
Under section 412(a) of the Plant Protection Act (7 U.S.C.
7712(a)), the Secretary of Agriculture may prohibit or restrict the
movement in interstate commerce of any plant or plant product if the
Secretary determines that the prohibition or restriction is necessary
to prevent the dissemination of a plant pest or noxious weed within the
United States. Based on information provided in the PRA and RMA, we
have determined that it is not necessary to prohibit the interstate
movement of citrus fruit from a quarantined area into States other than
commercial citrus-producing States under the conditions described in
the proposed rule. While APHIS has concluded that commercially packed
citrus fruit is an unlikely pathway for the introduction and spread of
citrus canker, the remaining uncertainty about the level of risk
associated with the movement of citrus fruit from a quarantined area
has led us to maintain the prohibition on the movement of citrus fruit
into commercial citrus-producing States.
One commenter supplied a report that provided initial data
demonstrating that transmission of Xac from infected fruit placed
directly under highly susceptible grapefruit seedlings does not occur.
The research (which can be viewed at http://www.regulations.gov/
fdmspublic/component/main?main=DocumentDetail&d=APHIS-2007-0022-0053)
is suggestive; when it is completed, it will help better determine
whether citrus fruit can serve as a pathway for the introduction of
citrus canker to commercial citrus-producing States outside the
quarantined area. We encourage interested parties to make research on
this issue available to us.
Two commenters stated that APHIS' treatment of the risk associated
with citrus canker was inconsistent with its treatment of the risk
associated with other plant pests. For example, one of the commenters
stated, the evidence is clear that the interstate movement of nursery
stock is a pathway for the long-distance spread of P. ramorum, but
APHIS' regulations continue to allow high-risk nursery stock to move to
all States, under specified conditions. The commenter cited APHIS'
actions with respect to the light brown apple moth as another example.
The provisions governing the movement of regulated articles for
each pest for which APHIS maintains quarantine requirements are the
result of separate considerations of the available science and the risk
posed by the plant pest in question. We make our determinations of risk
based on, among other things, the likelihood that a pest will follow a
specific pathway, the economic and environmental value of resources
that could be damaged by the pest, and the likelihood of introduction
of the pest into an unaffected area. Our choice of regulatory approach
is based on, among other things, the likelihood that the mitigations
available to us will be sufficient to prevent the introduction or
spread of a plant pest. We have determined that the level of protection
against the interstate spread of citrus canker that will be provided by
the regulations as amended by this final rule is appropriate.
One commenter asked why APHIS allows fruit to be exported from the
quarantined area into the citrus-producing areas of Europe, given that
we proposed to prohibit the distribution of fruit from quarantined
areas into commercial citrus-producing States. Other commenters asked
that we allow the interstate movement of fruit from quarantined areas
into commercial citrus-producing States under conditions similar to
those required by the European Union (EU) for the importation of citrus
fruit into the EU.
APHIS certifies U.S. plant products for export according to the
conditions set by the importing country for the exportation of those
products from the United States. The EU's requirements for the
importation of citrus fruit apply to all areas where citrus canker is
present, not just in the United States but in other countries whose
citrus production areas are affected by citrus canker.
The EU import requirements involve certification of grove freedom
from citrus canker and are similar to, but less restrictive than, the
requirements that were in the regulations before the publication of
this final rule. For reasons discussed in the RMA, we do not consider
these requirements to be sufficient to allow the movement of fruit from
citrus canker quarantined areas into commercial citrus-producing States
at this time. We will continue to review the available science and will
update the regulations if necessary.
Two commenters stated that Option 3, which would have allowed the
unlimited distribution of tangerines subject to treatment and APHIS
inspection, should be implemented. One commenter stated that canker
finds have been few and far between, if the disease has been found at
all, on some varieties of tangerine. Another stated that mandarin
varieties are the least susceptible to citrus canker, and that the
commercial citrus-producing States of California and Texas are
important markets for producers of this fruit.
Tangerines are generally grouped in the species Citrus reticulata
and are widely regarded as less susceptible to citrus canker disease
than other commercially grown Citrus species. But many of the
``tangerine'' varieties grown in Florida are hybrids of C. reticulata
with other more susceptible Citrus species. Clearly, tangerines in
Florida are not immune to citrus canker, as APHIS records indicate
that, during the 2005-2006 growing season grove surveys, Xac was
detected on 274 samples from tangerine, tangor, and tangelo groves.
APHIS pest interception data indicate that between 1985 and
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2006, Xac was intercepted 632 times on C. reticulata fruit. The level
of susceptibility was expressed as a continuum across ``tangerine''
varieties rather than as a discrete immunity for all varieties. This
creates a regulatory problem when an overlap occurs in the level of
susceptibility expressed by, for example, a more susceptible tangerine
variety and a more resistant nontangerine citrus variety. Sufficient
evidence does not exist to exclude tangerines from regulations
applicable to other Florida citrus varieties. We are making no changes
to the proposed rule in response to these comments.
Several commenters supported Option 4 but asked APHIS to continue
to examine the scientific evidence with a view toward allowing
unlimited distribution of fruit moved interstate from areas quarantined
for citrus canker at some future time.
We will continue to examine scientific evidence regarding whether
commercially packed citrus fruit (both with and without visible canker
lesions) is an epidemiologically significant pathway for the
introduction and spread of citrus canker. If, in the future, evidence
is developed to support a determination that commercially packed citrus
fruit is not an epidemiologically significant pathway for the
introduction and spread of citrus canker, we would undertake rulemaking
to amend our regulations accordingly.
Some commenters proposed other options to allow the movement of
fruit from quarantined areas. One commenter stated that fruit from
groves that are free of citrus canker and that are 1,500 feet or
farther from an affected grove should be allowed to move fruit to
commercial citrus-producing States.
It has been our experience in the State of Florida that citrus
canker can spread more than 1,500 feet in stormy conditions. We
recognize that citrus canker-free areas may exist adjacent to infected
areas, but implementing the commenter's suggestion would require grove
certification programs similar to those in place prior to the
publication of this final rule. We have determined that certification
of fruit for interstate movement at the packinghouse level rather than
at the grove level will ensure an appropriate level of phytosanitary
security; would be more reliable and less easily circumvented than the
preharvest grove survey required by Option 5; would be consistent with
the risk associated with citrus canker and commercially packed fruit
from Florida; and would be easier and potentially less costly to
implement and enforce than a grove-centered system of mitigations.
Some commenters disagreed with our determination that prohibiting
the distribution of citrus fruit from a quarantined area into
commercial citrus-producing States would be an effective mitigation.
Commenters holding this view stated that the illegal movement of citrus
fruit harboring citrus canker from a quarantined area to a commercial
citrus-producing State may be expected through current commercial
channels; they cited the movement of Spanish clementines from Georgia
to Florida through retailer distribution when such movement was
prohibited as one example of the potential for incorrect distribution.
Another commenter cited the discovery of Florida fruit in commercial
citrus-producing States as a result of distribution mistakes.
These commenters also stated that the potential for the movement of
Florida citrus by tourists and visitors from nearby States into
commercial citrus-producing States should also be taken into account,
and that excluding shipments to buffer States would reduce the risk
that this movement poses to commercial citrus-producing States. One
commenter stated that the history of citrus disease movement such as
citrus canker and citrus greening into Florida shows the high risk of
movement by plant or by fruit from other citrus-growing countries. In
these cases the initial infections were in urban areas, but movement to
production areas was undetected until an epidemic was finally observed.
One commenter also stated that we had not addressed mail-order
shipment or gift-pack movement of citrus from Florida.
These commenters proposed that we limit the distribution of fruit
from citrus canker quarantined areas to other States in addition to the
commercial citrus-producing States, thus creating a ``buffer zone''
around the commercial citrus-producing States. The buffer zones
proposed by the commenters varied:
One commenter suggested that only States east of the
Mississippi River should be eligible to receive fruit moved interstate
from quarantined areas.
Two commenters suggested that only States in the northern
tier of the United States and east of the Mississippi River should be
eligible to receive such fruit.
Two others suggested a buffer zone of all the States
surrounding the commercial citrus-producing States.
We do not agree that a buffer zone, such as these commenters
suggest, is appropriate or necessary. Due to the geographic separation
between Florida and other commercial citrus-producing States, citrus
canker is not likely to spread through natural means (such as through
storms) from Florida to a State that is not a commercial citrus-
producing State and then to a commercial citrus-producing State. While
it is correct that the movement of plants for planting presents a high
risk of spreading citrus canker from a quarantined area, the
regulations already contain a prohibition on the movement of plants for
planting; currently, only calamondin and kumquat plants are allowed to
move interstate from the quarantined area, and those plants must be
produced under conditions designed to prevent their infection with
citrus canker. As mentioned earlier, we have determined that it is
unlikely that the movement of commercially packed citrus fruit is an
epidemiologically significant pathway for the spread of citrus canker.
The proposed rule included requirements that boxes or other
containers of fruit moving interstate from a quarantined area include a
limited permit mark as well as the statement indicating that the fruit
is not to be distributed into a commercial citrus-producing State. This
requirement (which applies to mail-order and gift-pack shipments as
well as truck shipments) will help to prevent inadvertent movement of
citrus from quarantined areas into a commercial citrus-producing State.
To strengthen the protection provided by the limited permit
requirement, we are also adding a requirement in this final rule that
the limited permit mark and the distribution statement appear on any
shipping documents accompanying boxes or other containers in which
fruit is moved interstate.
To ensure that regulated parties comply with distribution
restrictions, APHIS routinely monitors wholesalers and fresh fruit
markets in commercial citrus-producing States and monitors distribution
routes that are bound for commercial citrus-producing States to ensure
that Florida citrus fruit does not unlawfully enter those States. This
monitoring is conducted primarily by APHIS' Smuggling, Interdiction,
and Trade Compliance program.
If we find Florida citrus in a commercial citrus-producing State,
we will trace the product back to its distributor and its origin in
Florida. We will investigate violations (through APHIS' Investigative
and Enforcement Services) and may seek penalties against any
distributor that moves Florida citrus to commercial citrus-producing
States. We may seize the prohibited products and destroy them or ensure
they are moved from the area of concern. We
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will conduct surveillance on other methods of sale such as Internet
sales and gift-pack shipments to ensure that the fruit is not
advertised as being available for delivery to commercial citrus-
producing States. We will also provide outreach to retailers and
wholesalers who are moving products to help prevent any inadvertent
movement of citrus from a quarantined area into a commercial citrus-
producing State.
The packinghouse measures of disinfection and APHIS inspection
ensure that even if a given shipment were illegally moved to a
commercial citrus-producing State, the shipment would have a low
likelihood of containing fruit with the potential to cause an outbreak
of citrus canker disease.
As mentioned earlier, the RMA examined four options for allowing
the interstate movement of citrus fruit from a citrus canker
quarantined area under a packinghouse-centered approach. Of those four
options, we determined that Option 4 was most appropriate, based on the
available scientific evidence, which indicates that fruit subject to
commercial packing, treatment, and APHIS inspection will be unlikely to
serve as a pathway for the introduction or spread of citrus canker.
We recognize that individual consumers may move fruit from Florida
into States other than commercial citrus-producing States and then
subsequently move that fruit into commercial citrus-producing States.
However, such movement could have occurred under the regulations in
place before the publication of this final rule as well; APHIS does not
have the regulatory infrastructure to monitor interstate movement of
fruit by individual consumers. Additionally, even with a buffer zone in
place, tourists and visitors would often travel across multiple States
to reach their destinations, meaning that a buffer zone would not be
highly effective at eliminating this consumer movement. For tourists
and visitors, as well as for local residents who routinely move between
commercial citrus-producing States and other States, the distance
between the borders of commercial citrus-producing States and the
citrus-producing areas within those States acts as a buffer as well,
further decreasing the risk associated with such movement. Finally, the
volume of such movement is extremely low when compared with the volume
of commercial movement of fruit, making the risk of citrus canker
establishment in commercial citrus-producing States through this
scenario highly unlikely. These factors, combined with our
determination that the introduction and spread of Xac into other
commercial citrus-producing States through the movement of commercially
packed fresh citrus fruit is unlikely and that the mitigations of
treatment and APHIS inspection are highly effective, have led us to
determine that a buffer zone to address such movement is unnecessary.
Scientific Evidence Used in the PRA and RMA
We received several general comments on the scientific evidence we
used to make our determinations in the PRA and RMA. One commenter
stated that the conclusion reached by the RMA is in part based on the
lack of evidence that citrus fruit could play a role in the
introduction of citrus canker in new areas, but that this lack of
evidence is a consequence of the lack of scientific studies and is not
based on scientific data; this commenter suggested that we evaluate the
risks further using fruit produced subject to the regulations that were
in place before the publication of this final rule. Another commenter
suggested an extensive list of experimental data that the commenter
believed were necessary to prove that the introduction and spread of
Xac into other commercial citrus-producing States through the
interstate movement of commercially packed fresh citrus fruit from a
quarantined area is unlikely. One commenter stated that this program,
which the commenter characterized as precedent-setting, requires a much
more solid foundation of science and process affirmation than has been
developed to date. Other commenters stated that not enough of the
evidence we used in developing the RMA had been published in peer-
reviewed scientific journals and that we had relied too much on
preliminary research in making our determinations.
We used the best scientific evidence available to develop the PRA
and the RMA, and we have detailed extensively how this evidence
supports the conclusions we present in those documents. It is important
to note that, based on the available evidence, we did not conclude that
commercially packed citrus fruit could not serve as a pathway for the
introduction and spread of Xac, but rather that it was unlikely that
commercially packed citrus fruit serves as an epidemiologically
significant pathway. That is why this final rule prohibits the
distribution of such fruit to commercial citrus-producing States.
The Plant Protection Act charges us with ensuring that our
decisions affecting imports, exports, and interstate movement of plants
and plant products that we regulate under the Act are based on sound
science. To fulfill this mission, we use all the scientific evidence
that may be brought to bear on an issue, not just studies published in
peer-reviewed journals. Observations based on APHIS' experience, survey
and pest detection data, and preliminary experimental results can all
provide valuable information to inform a regulatory decision, and we
have used them in the PRA and RMA when appropriate. Having said that,
the vast majority of the sources cited in the PRA and RMA have been
peer-reviewed, as have both the PRA and RMA themselves.
Comments on specific studies we cited in the RMA and PRA are
discussed later in this document.
The peer review for the RMA was conducted concurrently with the
comment period for the proposed rule. One commenter stated that
stakeholders should have the opportunity to review the peer reviewers'
comments when submitting their own comments on this document.
We appreciate the commenter's concerns. APHIS had already provided
for peer review of and public comment on the PRA, which informed the
development of the RMA. In accordance with the Office of Management and
Budget's bulletin on peer review, we are also making all the materials
associated with the peer review, including the peer reviewers'
comments, available at http://www.aphis.usda.gov/peer--review/peer--
review--agenda.shtml. The conclusion of the RMA did not change as a
result of the peer review, which was generally favorable.
One commenter included a late comment on the PRA as a reference,
stating that APHIS had not made appropriate changes to the PRA based on
the comment.
We reviewed the comment that the commenter included when we
developed the revised version of the PRA. We addressed all the
substantive points raised by that comment in the revised version of the
PRA published with the proposed rule. Many of the points raised by that
comment had been previously raised in other comments submitted on the
PRA during the comment period.
As discussed earlier, the PRA concluded that asymptomatic,
commercially produced citrus fruit treated with a surface disinfectant
and subject to other mitigations is not epidemiologically significant
as a pathway for the introduction and spread of citrus canker. However,
in order to apply the conclusions of the PRA, we determined that we
needed to extend its application to evaluate methods by
[[Page 65177]]
which fruit could be produced, treated, inspected, packaged, and
shipped without resulting in the spread of citrus canker to commercial
citrus-producing areas. Accordingly, the RMA addresses the risk
associated with all commercially packed fruit; the RMA's
recommendations have served as the basis for the Secretary's
determination that it is not necessary to prohibit the interstate
movement of citrus fruit from a quarantined area into States other than
commercial citrus-producing States under the conditions described in
the proposed rule. Therefore, specifically addressing comments on the
PRA is unnecessary for the purposes of this rulemaking.
The Packinghouse-Centered Approach and the Current Regulations
In evaluating the risk associated with asymptomatic fruit, the PRA
assumed that the citrus fruit in question was commercially produced
under a specific set of pest management measures. The RMA, while
recognizing that effective pest management measures for Xac are
available to private and commercial growers and are normal production
practices for many of these growers, does not assume that measures in
the grove are mandatory. Instead, the RMA focuses on treatment with an
APHIS-approved disinfectant at the packinghouse and APHIS inspection of
fruit to be moved interstate. The recommendations in the RMA served as
the basis for the proposed rule.
The regulations in place at the time the proposed rule was
published required that fruit moved interstate originate in a grove
that was found by an inspector to be free of citrus canker no more than
30 days before harvest (with additional requirements for limes), in
addition to treatment of vehicles, equipment, and other articles that
are used on the grove and treatment of the fruit itself.
Several commenters objected to APHIS moving away from the grove
inspection approach and to the fact that we did not propose to require
the use of the commercial production practices described in both the
PRA and the RMA. These commenters stated that, under the proposed rule,
measures such as copper sprays, designation and exclusion of infected
trees, field culling of fruit, and packinghouse culling of fruit were
all voluntary, and their effectiveness was unknown. The commenters
expressed concern that not requiring these measures would increase the
risk associated with citrus fruit moved interstate from a quarantined
area.
One commenter stated that in other countries such as Argentina that
ship fruit to citrus-producing countries in Europe, strict guidelines
are followed that include field inspections and the planting of wind
breaks between orchards that minimize wind velocity and subsequent
dispersal of inoculum. The commenter stated that these countries
realize that inspection of ``finished'' fruit in the packinghouse alone
is not enough to guarantee the shipment of disease-free fruit.
One commenter stated that the objective of a rule addressing
Florida's situation should be to prevent citrus canker from being
introduced into disease-free areas in the United States; such a rule
should not be designed with the primary objective of allowing shipments
of fresh fruit from canker-affected areas. This commenter stated that
the building blocks of premises and assumptions set forth in the
proposed rule and the RMA create risk rather than develop protective
barriers.
The regulations promulgated in this final rule include protective
barriers against the introduction of citrus canker into other citrus-
producing areas: Treatment with a surface disinfectant, APHIS
inspection, and a prohibition of the movement of citrus fruit from a
quarantined area into commercial citrus-producing States. We have
determined that these barriers provide an appropriate level of
protection with regard to the movement of citrus fruit from areas
quarantined for citrus canker.
The grove certification requirement in place prior to the
publication of this final rule and the APHIS packinghouse inspection
required under this final rule are not dissimilar in their approach to
preventing the interstate movement of fruit with visible canker
lesions. Under the regulations in place before the publication of this
final rule, none of the grove-centered measures cited by the commenters
(copper sprays, designation and exclusion of infected trees, and field
culling of fruit) were required. Rather, growers were required to
demonstrate that their groves were free from citrus canker, on the
basis of an inspection. In order to be found free from citrus canker,
and thus have fruit from their groves be eligible for the interstate
market, growers had incentives to employ the grove-centered measures
described in the PRA and RMA and mentioned by the commenters.
Instead of a grove inspection, this final rule requires an
inspection of the finished fruit at the packinghouse, which must
operate under a compliance agreement and treat fruit with an approved
surface disinfectant. Every lot of fruit must be inspected by an APHIS
inspector for visible canker lesions. While growers are not required to
practice measures that would reduce the prevalence of citrus canker in
their fruit, and packinghouses are not required to perform their own
culling process to remove fruit with visible canker lesions, the
regulations promulgated in this final rule still provide them with a
strong incentive to do so, since lots of fruit that fail APHIS
inspection will not be eligible for interstate movement. Additionally,
packinghouse culling for blemished fruit of any kind is already a
standard business practice, and field management programs that include
the use of copper sprays and field sanitation are already available to
producers.
The purpose of the APHIS inspection at the packinghouses is to
ensure that fruit moved interstate is free of visible canker lesions,
and to prohibit the interstate movement of fruit that is not free of
those lesions. From each lot of fruit intended for interstate movement,
APHIS will inspect a quantity that is sufficient to detect, with a 95
percent level of confidence, any lot of fruit containing 0.38 percent
or more fruit with visible canker lesions. Lots of fruit that fail
inspection will not be allowed to enter interstate commerce.
A packinghouse-based inspection can ensure an appropriate level of
phytosanitary security and will be easier to implement and enforce than
the grove certification system in place before the publication of this
final rule. Because it focuses on the end product, a packinghouse-based
inspection will be more reliable and less easily circumvented than the
preharvest grove survey that has been required in the regulations. A
packinghouse-based inspection is also consistent with the risk
associated with citrus canker and commercially packed fruit from
Florida. In addition, a phytosanitary packinghouse inspection creates a
performance standard for packed fruit that allows citrus producers
greater flexibility to determine the most efficient and effective means
of producing a compliant product.
Our choice of a packinghouse-based APHIS inspection as a means to
prevent fruit with visible canker lesions from being moved interstate,
rather than requiring specific grove and packinghouse practices to
ensure the production of fruit free of visible canker lesions, is
consistent with the recommendations of the 1997 Presidential/
Congressional Commission on Risk Assessment and Risk Management. The
commission recommended that agencies use alternatives to command-and-
control
[[Page 65178]]
measures that dictate the use of specific technologies, where
applicable (CRARM 1997), in order to encourage flexibility in the
choice of risk management alternatives.
One commenter characterized the approach of the proposed rule as a
control point approach, and stated that in the past APHIS has applied
control point approaches only to quarantine treatments that are able to
demonstrate a probit 9 level of effectiveness.
The probit 9 standard (99.997 percent mortality) applies to
treatments for insect pests such as fruit flies, not to treatment of
pathogens. In any case, the probit 9 standard is not applicable for the
surface disinfectant treatment and packinghouse-based APHIS inspection
that we are requiring. Scientific evidence indicates that both of these
measures are highly effective.
One commenter stated that the PRA and RMA appeared to imply that
packinghouse studies conducted to date were based upon fruit with known
levels of contamination with Xac. The commenter asked how the
packinghouse inspection process would achieve the results described in
the RMA without grove inspections and without the ability to determine
the infection pressure. The commenter also asked how the proposed
measures can be effective without knowing the magnitude of the hazard,
as expressed by the proportion of infected fruit.
Both of the packinghouse measures that we are requiring in this
final rule are effective regardless of infection pressure. The surface
disinfectant treatments approved by APHIS reduce numbers of Xac cells
to low or undetectable levels. The APHIS packinghouse-based inspection
is sufficient to detect, with a 95 percent level of confidence, any lot
of fruit containing 0.38 percent or more fruit with visible canker
lesions. In other words, if the infection pressure is higher than 0.38
percent of the fruit, it is 95 percent likely that the lot will be
rejected from interstate commerce.
Two commenters cited findings of canker symptoms on fruit exported
from Argentina and Uruguay to Spain in stating that symptomatic fruit
will often pass through the packinghouse process. These commenters
stated that the price growers and packers are receiving for citrus is
what drives the quality of the citrus shipped, and that with low
prices, low-quality fruit, such as those with canker, are more likely
to be introduced into distribution channels.
We agree that, in general, price helps to determine the quality of
fruit supplied. However, under the regulations established by this
final rule, the fruit will be subject to an additional APHIS inspection
separate from any field inspection and culling or packinghouse culling
that may occur. Any lot that fails APHIS inspection will not be
approved to move for interstate commerce. Given that, if there is a
financial advantage to being able to supply fresh citrus to the
interstate market, producers and packinghouses in quarantined areas are
likely to employ measures and processes that will allow them to supply
fruit free of visible canker lesions for APHIS inspection.
Treatments and Surface Contamination With Xac
The regulations require all fruit moved interstate from an area
quarantined for citrus canker to be treated in accordance with Sec.
301.75-11(a). This paragraph has included two treatments: Thorough
wetting for at least 2 minutes with a solution containing 200 parts per
million (ppm) sodium hypochlorite, with the solution maintained at a pH
of 6.0 to 7.5; or thorough wetting with a solution containing sodium-o-
phenyl phenate (SOPP) at a concentration of 1.86 to 2.0 percent of the
total solution, for 45 seconds if the solution has sufficient soap or
detergent to cause a visible foaming action or for 1 minute if the
solution does not contain sufficient soap to cause a visible foaming
action.
One commenter noted that disinfectants are only effective if the
active ingredient is not degraded. The commenter gave the example that
sodium hypochlorite is degraded by sunlight and organic matter.
We agree with the commenter's point that it is important to ensure
that the treatment is conducted properly. APHIS regularly monitors the
treatment of fruit to ensure that the disinfectant agent is at the
proper concentration and, in the case of sodium hypochlorite, pH, thus
ensuring the effectiveness of the treatment. Under this final rule, we
will conduct monitoring under conditions specified in the compliance
agreements with packinghouses.
In this final rule, we are amending the treatment regulations to
require fruit to be treated at a commercial packinghouse whose owner
operates under a compliance agreement. Previously, the regulations had
required that treatment be performed either in the presence of an
inspector or at a facility whose owner operates under a compliance
agreement under Sec. 301.75-7(a)(2); this change will reflect the fact
that all fruit intended for interstate movement must be treated at a
commercial packinghouse under this final rule.
Several commenters stated that these surface disinfectant
treatments may not be 100 percent effective, citing various reports
that indicated that bacteria could be recovered from citrus fruit that
had been treated with sodium hypochlorite or SOPP, including reports by
Verdier (2006) and Golmohammadi (2007) and a newspaper article
reporting on a lecture by Gottwald in which he presented unpublished
preliminary results. With regard to the last of these, two commenters
requested that we provide information about the followup studies
mentioned in the article.
As stated in the RMA, the surface disinfectant treatments approved
by APHIS reduce numbers of Xac cells to low or undetectable levels, but
do not necessarily provide complete eradication. The evidence cited by
the RMA does demonstrate that the treatments allowed under the rule
substantially reduce bacterial populations, including Xac, found on the
surface of citrus fruit to the extent practicable using surface
disinfectant treatments currently registered for use in the United
States on raw fruits and vegetables.
Recovery of Xac from fruit after surface disinfectant treatment
does not demonstrate that the treatment is ineffective. Microbial
detection or recovery tests simply measure the presence or absence of
the organism in a sample and do not enumerate or measure the difference
between the pre- and post-treatment bacteria population levels or
infectivity. The treatments in the regulations are consistently
reported as dramatically reducing Xac populations on the surface of
fruit, if not eliminating them entirely. For example, Verdier (2006),
cited by the commenters, measured the pre- and post-treatment levels in
the wash solution and found that the bacteria population level was
reduced 99.8 percent from an average of 39.4 colony-forming units
(cfu)/mL on untreated controls to an average of 0.06 cfu/mL on treated
fruit.
The information from Gottwald (2006) the commenters cite has not
been published, and the followup studies referred to in news reports
are currently being completed. We are not able to obtain the
unpublished data that have been collected to this point. We will review
the Gottwald information when it becomes available in final form. It is
important to note again that the recovery of some bacteria after
treatment is not inconsistent with treatment being highly effective at
reducing Xac population levels, as described earlier.
Another commenter, referring to a study by Brown and Schubert
(1987)
[[Page 65179]]
that the RMA cited, stated that the study's use of Xanthomonas
campestris pv. vesicatoria as a proxy for X. axonopodis pv. citri in
assessing the efficacy of SOPP was not appropriate, because the
behavior of closely related bacteria may be very different.
The use of a proxy in efficacy testing is not unusual; for example,
the Environmental Protection Agency (EPA) requirements for testing the
efficacy of disinfectants allow the use of a proxy. A proxy organism
was used in this study because the study was conducted in a model
packinghouse. It is difficult to experiment with quarantine plant
pathogens in the field because of the need to provide safeguards
against their spread. While the bacteria in question are not identical,
SOPP has a broad range of efficacy; there is no reason to believe that
some feature of Xac would defeat the mechanism of SOPP. In addition,
the RMA cited other studies establishing the efficacy of SOPP as a
treatment against Xac itself.
The PRA contained the following statement regarding treatment
effectiveness: ``Studies performed in Argentina on the effectiveness of
sodium hypochlorite on mature symptomless fruit artificially
contaminated with Xac showed that sodium hypochlorite levels as low as
8 ppm were effective in eliminating epiphytic or surface bacteria from
the fruit (Canteros, undated).'' One commenter stated that there were
no references about the viability of the bacteria, which is an
important factor for risk assessment.
This particular study was one of many studies cited in the PRA and
RMA establishing the effectiveness of sodium hypochlorite as a
treatment. Other studies we cited included references about the
viability of the bacteria.
Related to the presence of bacteria on the surface of treated fruit
(also referred to as epiphytic bacteria or contamination), several
commenters stated that fruit with such populations pose a risk of
spreading citrus canker that was not addressed by the measures
recommended in the RMA.
While surface populations of Xac undoubtedly exist on some citrus
fruit that is packed in a quarantined area, and commenters cited
scientific evidence establishing this point, substantial evidence
indicates that surface bacterial populations do not infect mature fruit
or survive on mature fruit long enough to infect other hosts. The
evidence cited in the RMA regarding epiphytic survival indicates that
epiphytic populations on harvested, mature fruit decline rapidly. For
example, researchers in Brazil sprayed asymptomatic fruit, picked from
trees, with a bacterial suspension of 106 cfu/mL; no
bacteria were recovered after 5 days at room temperature under
laboratory conditions (Belasque and Rodriguez Neto 2000). Epiphytic
bacteria do not multiply in water on leaf surfaces or on dry leaves
(Timmer et al. 1996). Graham et al. (2000) found that Xac survived for
48 to 72 hours on a variety of inanimate surfaces in sun or shade,
respectively. Additionally, there is no authenticated record of
movement of diseased fruit as the origin for a citrus canker disease
outbreak, which is especially suggestive given the brisk global trade
in such fruit and the likely presence of some level of epiphytic
bacteria on many fruit that is exported from citrus canker-affected
areas.
Commenting on the PRA, one commenter noted that a low concentration
of 8 cfu/mL (cited as a result of treatment by one study) may mean very
high numbers of bacteria in tons of fruit.
The commenter's assertion is correct. However, shipments of fruit
are commercially packed in boxes or other approved containers and are
dispersed through market channels all over the United States, greatly
diluting the concentration of bacteria which are at the same time
experiencing rapid mortality. Therefore, such bacterial concentrations
would not occur in the real world. In any case, for the reasons stated
above, we have determined that fruit with epiphytic bacterial
populations is not an epidemiologically significant pathway for the
spread of citrus canker.
Some commenters were also concerned about the possible presence of
Xac on other materials, citing reports of Xac survival for various
periods on media like clean microscopic slides; leaf surfaces, plastic,
wood, and other materials; cloth, sawdust and shavings, dried herbarium
tissue, and sterile soil; and non-host weeds.
While Xac undoubtedly persists on a number of surfaces, it does not
multiply outside of hosts. Under the regulations, the interstate
movement of any regulated article other than fruit, calamondin and
kumquat plants, and seed is prohibited. Regulated articles include
leaves and grass clippings. In addition, under paragraph (c) of Sec.
301.75-3, an inspector may designate any other product, article, or
means of conveyance, of any character whatsoever as a regulated article
when it is determined by an inspector that it presents a risk of spread
of citrus canker and the person in possession thereof has actual notice
that the product, article, or means of conveyance is subject to the
provisions of this subpart. We do not typically regulate the movement
of the other articles cited by the commenters under the current
regulations because populations of Xac on such articles are very
unlikely to infect mature citrus fruit.
Two commenters were concerned about the possibility that canker-
infected fruit could contaminate packinghouse equipment with Xac. One
commenter stated that packinghouse equipment needs to be disinfected if
citrus canker is found in a lot run on that equipment. The other
expressed a specific concern about contamination of existing wounds in
fruit and stated that surface disinfestation cannot be continuously
done during the commercial packing of fruit where both diseased and
healthy fruit are being packed. This commenter suggested that we amend
the regulations to exclude fruit from being packed from orchards or
harvested fruit lots with an incidence of citrus canker above some
established threshold, in order to minimize contamination of packing
lines.
We acknowledge that infected fruit in a lot could contaminate the
packing line with Xac, but, as stated above, substantial evidence
indicates that the epiphytic bacterial populations that could be
transferred from the packing line to the fruit do not infect mature
fruit or survive on mature fruit long enough to infect other hosts. For
that reason, we have determined that grove inspections are not
necessary to mitigate the risk associated with such contamination, nor
is disinfection of the packing line equipment necessary if canker is
found during the inspection of a lot of fruit.
The RMA stated that ``Bacteria within lesions may be more protected
from the detrimental effects of washing, disinfection and drying.
Viable Xac has been recovered by APHIS pathologists from citrus canker
lesions on fruit culled from packinghouse lines after postharvest
treatments (Riley 2007).'' A few commenters expressed concern relating
to this statement. One stated that chlorine is well known as a surface
sanitizer but has no ability to penetrate beyond the surface--for
example, into lesions. Another commenter noted that none of the
experiments mentioned in the PRA or RMA evaluate the effect of
disinfectants on Xac within the fruit, either in visible lesions (of
any size) or in circumstances where the effects of Xac are not visible
to the naked eye. The third, reacting to the statement about recovery
of viable Xac by APHIS pathologists after postharvest treatments, asked
what treatment had been performed, what level of recovery
[[Page 65180]]
had occurred, what preharvest management the fruits were subject to,
why the fruits were not culled on the packing line before treatment,
and whether the postharvest treatment included wax.
As stated earlier, the surface disinfectant treatments required in
this final rule reduce numbers of Xac cells to low or undetectable
levels. The RMA acknowledges that treatment with surface disinfectants
is not effective on canker lesions, which is why this final rule also
requires an APHIS inspection of each lot of fruit for canker lesions.
The canker lesions referred to in Riley (2007) occurred in fruit
produced under the regulations that were in place before the
publication of this final rule, i.e., with certification of grove
freedom and with surface disinfectant treatment. As the regulations in
place before the publication of this final rule did not require
specific canker management measures, we do not have records of what
canker management measures the fruit may have been subject to beyond
the measures required by the regulations.
Addition of Peroxyacetic Acid Treatment
We proposed to add a new surface disinfectant treatment using
peroxyacetic acid (PAA). The proposed rule would have required the
regulated fruit to be thoroughly wetted for at least 1 minute with a
solution containing 85 ppm peroxyacetic acid. At the request of growers
in Florida, we evaluated the efficacy of this treatment and determined
that the disinfectant is at least as efficacious as a surface
disinfectant treatment as the currently approved disinfectants listed
in the regulations. In the RMA, we described the tests that had been
performed to confirm the efficacy of PAA. These tests were conducted on
X. axonopodis pv. citrumelo (Xa citrumelo), which was used as a
surrogate for X. axonopodis pv. citri (i.e., Xac).
Two commenters stated that PAA should be tested on Xac itself
rather than on a surrogate. One stated that Xa citrumelo does not
infect fruit and does not survive in orchards, making it a poor
surrogate, and asked that we make the data referred to in the RMA
publicly available. Another stated that, while it seems highly likely
that PAA may be effective against Xac, to allow its use without any
testing against the particular organism of concern appears to be
unnecessarily optimistic. The commenter recommended testing in field
conditions for this application or at least to demand post-introduction
testing to demonstrate efficacy in the field.
We are making the data on PAA testing available on the
Regulations.gov Web site with this final rule (see footnote 1 at the
beginning of this final rule) or from the person listed under FOR
FURTHER INFORMATION CONTACT.
As noted earlier in this document, the use of a proxy or surrogate
is not unusual when testing a treatment's efficacy on a quarantine
pathogen. The EPA label for PAA, which states the approved instructions
for use and applicability of the disinfectant, acknowledges that it was
tested on Xa citrumelo as a surrogate for Xac.
X. axonopodis pv. citrumelo and X. axonopodis pv. citri differ
primarily in the hosts they infect. (``pv.'' stands for ``pathovar,''
which distinguishes strains or subspecies of the same bacteria based on
their ability to only infect specific hosts.) X. axonopodis pv.
citrumelo is generally considered to be more resistant to disinfection
than X. axonopodis pv. citri, making the former a suitable surrogate
for the latter.
In addition, PAA is an oxidizing agent whose mode of action has
been shown to be effective on many bacteria, including Bacillus cereus,
B. subtilis, B. stearothermophilus, Clostridium botulinum, C.
butyricum, C. sporogenes, Ditylenchus dipsaci, Enterococcus faecium,
Escherichia coli (including E. coli O157:H7), Fusarium oxysporum,
Gluconobacter oxydans, Lactobacillus plantarum, L. thermophilus,
Leuconostoc mesenteroides, Listeria monocytogenes, Pseudomonas
aeruginosa, P. fluorescens, Saccharomyces cerevisiae, Salmonella
typhimurium, Staphylococcus aureus, Streptococcus delbreuckii subsp.
bulgaricus, and Yersinia enterocolitica. Based on PAA's characteristics
as a general disinfectant and the results of the testing on Xa
citrumelo, we have determined that PAA will be effective on Xac as
well, and we are adding PAA as a surface disinfectant treatment for
fruit in this final rule.
We are making three other changes related to PAA. While paragraph
(a) of Sec. 301.75-11 sets out treatments for fruit, paragraph (d) of
that section sets out requirements for treatment of vehicles,
equipment, and other articles. A solution of 85 ppm of PAA is also
effective when used on vehicles, equipment, and other articles, and the
availability of PAA as a treatment for packing line equipment would be
useful for packinghouses in the quarantined area to fulfill the
requirements in Sec. 301.75-7(c)(2)(iv) for disinfection of packing
equipment between packing lots of regulated fruit produced in a
quarantined area and packing lots of fruit not produced in a
quarantined area. Therefore, this final rule also adds PAA, when used
indoors, as an approved treatment for vehicles, equipment, and other
articles in paragraph (d) of Sec. 301.75-11. We may decide to add PAA
as a treatment for outdoor use in a separate rulemaking if we receive
requests to do so.
The proposed rule would have added PAA as a fruit treatment in a
new paragraph (a)(4) in Sec. 301.75-11. Paragraphs (a)(1) and (a)(2)
authorize the use of sodium hypochlorite and SOPP, respectively, as
treatments for fruit; paragraph (a)(3) requires that these two surface
disinfectants be applied in accordance with label directions. Instead
of adding PAA in a new paragraph (a)(4), we have redesignated paragraph
(a)(3) as (a)(4), added PAA in paragraph (a)(3), and amended paragraph
(a)(4) to indicate that PAA must be applied in accordance with label
directions as well.
The regulations in 7 CFR part 305 set out the requirements for
phytosanitary treatments. Section 305.11 contains the two treatments
that have been authorized for citrus fruit moved from a citrus canker
quarantined area. Accordingly, in this final rule, we are amending that
section to add PAA as a treatment for fruit.
Inspection and Potential for Mature Fruit Without Visible Lesions To
Serve as Pathway for Infection
As mentioned earlier in this document, the PRA examined the risks
associated with asymptomatic fruit. The PRA used the term
``asymptomatic'' to refer to the lack of visible signs or symptoms of
citrus canker. The RMA examined the risks associated with all fruit
that has been commercially packed, regardless of its disease status. We
also prepared a quantitative model (Appendix 1 to the RMA) based on
Florida production and shipping data to evaluate the efficacy of three
levels of phytosanitary inspection in ensuring that symptomatic fruit
does not enter commercial citrus-producing States. In the qualitative
model, we defined ``symptomatic'' as meaning that the fruit have
visible Xac lesions 1 millimeter (mm) in diameter and greater. One
commenter pointed out that these terms were used inconsistently in the
PRA and the RMA.
We appreciate the comment. In the version of the RMA that
accompanies this final rule, Appendix 1 refers to fruit that have
visible canker lesions and fruit that do not, rather than to
symptomatic and asymptomatic fruit.
[[Page 65181]]
This commenter further stated that the proposed APHIS inspections
of fruit target only relatively large symptoms readily visible to the
naked eye, not whether any bacteria are present on the fruit. While the
APHIS inspection is probably fairly effective at limiting the
occurrence of larger Xac lesions in marketed fruit, the commenter
stated, inspection is totally ineffective at detecting and limiting
lesions smaller than 1 mm or at detecting Xac-infected fruit that have
no visible lesions at the time of inspection. This commenter and other
commenters also addressed surface populations of bacteria, stating that
focusing inspection efforts on visible lesions ignores risk associated
with bacteria.
We addressed the risk associated with epiphytic bacterial
populations earlier in this document. We have determined that the other
situations described by these commenters are unlikely to occur outside
of an experimental setting. The reasoning behind this determination is
discussed below.
Small lesions (less than 1 mm). Commenters cited Koizumi (1972), in
which Satsuma mandarin were either prick inoculated with Xac or
naturally infected. The experimenter found that, in addition to lesions
greater than 1 mm, lesions referred to as ``late detection (small)'' of
a size of 0.1 to 0.15 mm also occurred. This would be below what we
have determined to be the size threshold for a detectable lesion, as
defined in Appendix 1 to the RMA. Besides stating that the existence of
such lesions indicates that fresh fruit could be a pathway for the
introduction or spread of citrus canker, the commenter also stated that
it is possible that disinfecting the surface of the fruit might
exacerbate the subsequent infectivity of Xac exuding from small
lesions, by removing other (e.g., rot-provoking) organisms that might
directly or indirectly accelerate the decline of Xac after harvesting.
As discussed in the RMA, in the field, immature citrus is most
susceptible to infection with Xac and lesion development. Mature citrus
fruit have natural wax layers on their surface, decreasing
susceptibility by reducing access to natural openings, such as stomata.
In addition, mature (not expanding) asymptomatic fruit without injuries
or blemishes are not known to develop symptoms in the field. In the
Koizumi (1972) study, mature fruit were experimentally inoculated while
the fruit was still attached to the tree; equivalent conditions are
extremely unlikely to occur naturally.
The lesions Koizumi observed resulted from a combination of
artificial (prick) inoculations and natural infections and therefore
provide little information about how the ratio of typical to atypical
lesions on fruit varies under natural conditions. Koizumi's results
varied greatly over the several years he conducted these experiments;
the commenters cite results from the year with the highest incidence of
infection, which coincided with unusually high temperatures and two
typhoons (hurricanes). Koizumi speculated that the atypical lesions
were the result of restricted expansion brought on by physiological
changes in the maturing fruit and lower ambient temperatures. As noted
by Graham et al. (1992b), the small late season lesions were
characterized by a ``lack of bacterial proliferation.'' Lesions without
proliferation would not provide an epidemiologically significant source
of inoculum for Xac infections.
While other studies have conducted similar inoculation tests on
fruit before (Fulton and Bowman 1929) and after (Graham et al. 1992b;
Verniere et al. 2003), Koizumi (1972) remains the only paper to
describe this type of lesion. Fulton and Bowman noted that if one was
not careful to avoid oil glands when making puncture inoculations, the
released oils cause injuries to the adjacent tissue. One could
speculate that at least some of Koizumi's atypical lesions might, in
fact, be injuries. We have no evidence that the lesions described by
Koizumi (1972) occur in nature and therefore cannot agree that they
would occur at the rates cited by the commenters.
Nevertheless, conditions could exist in which small Xac lesions
occur. However, as noted above, immature fruit are most susceptible to
Xac infection, and Xac lesions grow as the fruit matures; the growth of
the lesions slows as the fruit reaches maturity. Picking mature fruit
from the tree causes senescence of the fruit and further inhibits
lesion development. Therefore, while small lesions might occur on
immature fruit, they would typically grow into larger lesions as the
fruit matures; if there were small lesions present on such fruit, it
would be likely that lesions larger than 1 mm would be present as well.
In general, APHIS inspectors do not see fruit with only lesions smaller
than 1 mm; small lesions occur in association with larger lesions
(Riley 2007).
The packinghouse culling and grading procedures are designed to
remove fruit with visible lesions and would result in removal of the
fruits likely to harbor the highest pathogen loads, and therefore
present the greatest risk of disease transmission. The APHIS inspection
after the packing process is completed will result in the rejection of
any lot of fruit that has visible canker lesions and will prevent that
lot from moving in interstate commerce.
Wounded fruit. One commenter cited Fulton and Bowman (1929), who
inoculated a mature grapefruit from the market and 75 days later tested
the grapefruit. The test indicated that there were ``something like
32,000 bacteria per puncture,'' although the fruit had not developed
external lesions. Another commenter stated that a general principle of
postharvest pathology is that surface disinfestation of fruit with
standard oxidizing chlorine washes will inactivate most microorganisms
from the surface of non-wounded fruit, but not from fruit wounds.
The grapefruit described in Fulton and Bowman (1929) was one of a
number of market fruit that were inoculated in this way, the rest of
which either rotted after inoculation or supported bacterial
populations that did not multiply. All these fruits were kept in moist
laboratory conditions designed to facilitate the development of Xac
bacteria.
Regarding the grapefruit, Fulton and Bowman stated the following in
their 1929 study: ``There is apparently a very marked difference in the
behavior of the canker organism following inoculations in the peel of
mature fruit after removal from the tree as compared with its behavior
in the peel of mature fruit still on the tree. Possibly changes in the
physiological condition of the fruit resulting from its removal from
the tree are responsible for the difference * * * senescent changes in
the peel favor the development of fungi having saprophytic tendencies;
it is not inconsistent to presume these changes would in equal degree
hinder the development of an organism having definitely parasitic
habits like Pseudomonas citri [Xac].'' This is consistent with a
determination that infected wounds would occur extremely rarely in
real-world conditions.
Fulton and Bowman also reported that infection only occurred if the
wound stayed moist until the time of inoculation. Wounds that were
allowed to dry and were inoculated after 26 hours did not result in
infection. That is, infections occurred only when oil glands were
avoided and inoculum was applied within 26 hours of wounding (Fulton
and Bowman 1929). Verniere et al. (2003) reported a disease incidence
of zero when inoculating mature fruit either by pin prick or spray
inoculation.
As noted above, the conditions that would allow citrus canker to
develop in wounds in the field are unlikely to
[[Page 65182]]
occur. In addition, any fruit with wounds would likely be culled in the
field or by the packinghouse before it could be submitted for APHIS
inspection.
Based on this evidence, we have determined that fruit with small
lesions or infected wounds would occur extremely rarely and are not
likely to be epidemiologically significant when they do appear.
Therefore, it is appropriate to focus our inspection efforts on
detecting lesions 1 mm or greater.
The RMA stated that APHIS plant pathologists have intercepted fruit
in final packed cartons with lesions in the 2-3 mm range and have
observed that the majority of the symptomatic fruit that APHIS
inspectors intercepted after passing through the packing line
undetected by graders have only one lesion (Riley 2007). Two commenters
addressed this statement. Both asked for data on interceptions in
Florida fruit, with one asking for information on how many fruit were
detected and what varieties were found to be infected.
These data are available from the person listed under FOR FURTHER
INFORMATION CONTACT.
One commenter stated that the fact that APHIS inspectors
intercepted fruit with lesions did not substantiate the statement made
later in the RMA that grading and inspection procedures are effective
in removing fruit with visible lesions. Another commenter stated that
all canker infections cannot be detected in packinghouses without
knowing whether the fruit originates from a canker-free grove, or at
least a grove with a very low level of canker infection. The commenter
stated that it is very difficult, if not impossible, to distinguish
canker blemishes from numerous other blemishes, especially in the
growing conditions that prevail in Florida, where many blemishes appear
on fruit.
One commenter cited the example of citrus affected by septoria, a
fungus, that are exported to Korea. This commenter stated that the
California citrus industry conducts vigorous training programs for line
employees to identify and eliminate fruit with distinguishable symptoms
and that this culling is then augmented by laboratory analysis. The
commenter stated that lab analysis has always detected symptoms on a
small percentage of fruit missed by highly trained employees.
We appreciate the opportunity to clarify this point. Various
evidence, as cited in the RMA, indicates that packinghouse grading and
inspection procedures are effective in removing fruit with visible
lesions. Packinghouse graders and inspectors in Florida also receive
training provided by the State in identifying canker lesions. The
phytosanitary inspection that will be performed by APHIS in this final
rule will provide another layer of inspection protection. We provided
evidence supporting these points in the RMA, including detailed
evidence about the efficacy of APHIS' inspection process. Scientific
evidence indicates that these measures are highly effective, but since
uncertainty remains about the epidemiological significance of
symptomatic fruit, we are prohibiting the distribution of fruit moved
interstate to commercial citrus-producing States.
As discussed earlier in this document, the APHIS packinghouse-based
inspection is sufficient to detect, with a 95 percent level of
confidence, any lot of fruit containing 0.38 percent or more fruit with
visible canker lesions. In other words, if the infection pressure is
higher than 0.38 percent of the fruit, it is extremely likely that the
lot will be rejected from interstate commerce. APHIS inspection is thus
effective regardless of infection pressure.
One commenter, responding to both the evidence presented for APHIS
inspectors' detection efficacy in the qualitative portion of the RMA
and in the model in Appendix 1, stated that none of the evidence
provided for APHIS inspectors' detection efficacy corresponds to field
conditions for detection of lesions. The commenter noted that the cited
figures for refresher training correspond to identification within 40
seconds of a lesion presented to the inspector, which the commenter
stated was inconsistent with location of a rare lesion on a fruit in a
continuous search of 1,000 fruit samples within an average of 5
seconds, an estimate we presented in the Regulatory Impact Analysis for
the proposed rule in the context of describing the proposal's potential
impact on packinghouse operations. The commenter stated that evaluation
of enzyme-linked immunosorbent assay (ELISA) Dip Stick tools and the
evaluation of a diagnostic tool (if that is a separate exercise from
the ELISA Dip Stick tool) also corresponded to classification of
already-detected lesions.
We appreciate the opportunity to clarify the evidence presented in
the RMA on the APHIS phytosanitary inspection. The evidence provided in
the RMA is consistent with the proposed rule's approach of using
inspection to detect lesions in the packinghouse. The training for
phytosanitary inspectors was done in packinghouse conditions, using
culled fruit for the test sample. Both in training and testing and in
the packinghouse, inspection is performed on fruit that has been
removed from the packing line.
Under packinghouse conditions, there is no time limit for fruit
inspection once the fruit is randomly sampled. This can be accomplished
because the fruit is inspected individually, away from the packing
line. The 40-second time limit during training is a performance
requirement for training, not a packinghouse inspection requirement.
The estimate that the packinghouse inspection would require 5 seconds
per fruit is also not an APHIS packinghouse inspection requirement;
rather, this figure was cited in the context of the potential economic
impact of the lot inspection on the packinghouse, and specifically in
discussing possible delays associated with inspection. Inspectors who
see questionable lesions will be able to take whatever time is
necessary to determine whether those lesions are canker lesions.
The ELISA Dip Stick test did correspond to already detected
lesions. The results of the ELISA Dip Stick test were cited in the RMA
to provide empirical data on the size of lesions that can be detected
by inspectors. The ELISA Dip Stick test is not part of the detection
system that will be used in commercial packinghouses under this final
rule; it will be used only for confirmation of lesions found by
inspectors.
One commenter disagreed with the idea that only ``finished'' fruit
would be inspected for citrus canker in the packinghouse. The commenter
stated that citrus canker is more easily detected on fruit that has not
been through the packing process. Brushing of fruit on the packing line
may remove diseased tissue, the commenter stated, and waxing of the
fruit will make the disease harder to diagnose.
Inspection of fruit before they go through the packing process
would not allow the packinghouses themselves to cull canker-infected
fruit prior to packing. In the RMA, we described in detail the efficacy
of inspection of finished fruit for citrus canker, as discussed
earlier.
Our experience indicates that washing fruit will make it easier to
detect citrus canker lesions. Citrus fruit that comes directly from the
field is often covered in dirt, sooty mold, and other debris and
material that could obscure citrus canker lesions. Washing the fruit
removes some of this material. Because citrus canker lesions occur
within the peel of the fruit, they would not be brushed off during
finishing. Additionally, the wax used on fruit is transparent, which
means it would not impede disease detection.
[[Page 65183]]
Potential Pathways for Spread of Citrus Canker Through Movement of
Fruit
As mentioned earlier, the RMA that was made available with the
proposed rule concluded that the introduction and spread of Xac into
other commercial citrus-producing States through the movement of
commercially packed fresh citrus fruit is unlikely because:
Fresh citrus fruit is produced and harvested using
techniques that reduce the prevalence of Xac-infected fruit;
Citrus fruit is commercially packed using techniques that
reduce the prevalence of infected or contaminated fruit, including
disinfectant treatment for epiphytic contamination;
For a successful Xac infection that results in disease
outbreaks to occur an unlikely sequence of events would have to occur;
Reports of citrus canker disease outbreaks linked to fresh
fruit are absent; and
Large quantities of fresh citrus fruit shipped from
regions with Xac have not resulted in any known outbreaks of citrus
canker disease.
One commenter stated that we did not enumerate any complete
pathways for transmission and so did not evaluate the scientific
evidence in such a way as to evaluate the possibility or likelihood for
transmission along such pathways. The commenter also stated that there
are pathways (including illegal diversion of fruit and perfectly legal
amateur grower activities) from every part of the country that may lead
to infection of commercial citrus areas and that have not been
evaluated. This commenter and another commenter suggested several
potential pathways that we had not addressed in the RMA.
In general, it is difficult to examine quantitatively the pathways
by which infected fruit could theoretically spread citrus canker. Those
pathways are dependent on consumer behaviors and biological events for
which we lack data that we could use to quantify them, and no such data
were provided by the commenters. This lack of data is one reason we
have determined that it is appropriate to prohibit distribution of
fruit moved interstate from a quarantined area to commercial citrus-
producing States. As discussed earlier, such a prohibition, combined
with the monitoring and enforcement efforts APHIS will use to ensure
that the prohibition is adhered to, is effective at preventing the
illegal movement of fruit.
We discuss the specific pathways brought up by the commenters
below.
One commenter suggested that citrus canker could be spread through
long-distance movement due to storm or cyclone activity.
The available evidence indicates that the maximum range for spread
of citrus canker through storm activity would not be sufficient to
spread citrus canker from Florida to another commercial citrus-
producing State.
One commenter suggested that citrus canker could be spread through
movement on workers' clothes and picking bags.
As discussed earlier, while Xac can persist on a number of
surfaces, its infectivity outside lesions is unknown. We do not agree
that it is likely that workers will move between Florida and other
commercial citrus-producing States without laundering their clothes and
while carrying their own picking bags. The commenter provides no
evidence that could be used to empirically estimate the frequency of
such behavior, and APHIS is unaware of any such evidence.
Two commenters suggested that citrus canker could be spread if
fruit or peel from citrus fruit infected with Xac is placed in or
around susceptible host plants, after which a water event moves the
bacterium from the fruit or peel to the host plant. One commenter cited
Koizumi (1972) as evidence that Xac could be recovered from fruit peel
for months if the peel was placed in physiological solution for 2
hours. This commenter stated that only one bacterium is required to
cause infection. Another commenter cited fruit with live Xac cells that
are thrown into a compost pile or bin under a backyard citrus tree,
after which a splash or water movement occurs. Once a backyard citrus
plant was infected, these commenters stated, rain or storm events could
spread the bacterium to commercial citrus groves.
The Koizumi (1972) study recovered bacteria using physiological
solution, a buffered saline solution that ensures optimal conditions
for bacterial recovery. Analogous conditions do not occur in nature.
Additionally, for this scenario to occur, citrus fruit that is infected
would have to have been moved from a quarantined area into a commercial
citrus-producing State--movement that is prohibited by the regulations.
As discussed earlier, we are increasing monitoring and disease
surveillance activities and making changes to the regulations in order
to help prevent the illegal or inadvertent movement of fruit from
quarantined areas into commercial citrus-producing States. If an
infected fruit was illegally moved into a commercial citrus-producing
State, it would have to be exposed to susceptible plants under very
specific physical and environmental conditions for infection to occur.
While it is true that one bacterium is sufficient to cause
infection, that one bacterium would have to encounter conditions that
were appropriate for infection. There is a very low likelihood that any
one bacterium will encounter conditions sufficient to cause infection;
it is difficult to create these conditions even in a laboratory
setting. Under natural conditions, it would require thousands if not
millions of tries for one bacterium to cause infection. Gottwald and
Graham (1992) estimated that as few as 2.4 Xac bacteria forced into a
water congested stomatal cavity of a susceptible plant were sufficient
to cause a lesion. However, they also determined that the minimum
concentration of bacteria in the inoculum needed to produce an
infection, and presumably to place the estimated 2.4 bacteria in a
stomatal cavity, was 10\5\ cfu/mL. Thus, although it may take only 2.4
infective bacteria in the right place to cause infection, it takes
exponentially greater numbers of bacteria in the inoculum for those 2.4
bacteria to occur in the right place at the right time.
The data submitted by one commenter (see http://
www.regulations.gov/fdmspublic/component/
main?main=DocumentDetail&d=APHIS-2007-0022-0053), in which infected
fruit were placed next to grapefruit seedlings in natural conditions
for 2 months without infection of the seedlings, suggests that the
likelihood of such an occurrence may be low.
Finally, for this pathway to occur, rain or storm conditions would
have to prevail that could spread the bacterium over long distances,
but Borchert et al. (2007) concluded that such conditions are unlikely
to prevail outside Florida, the State that is currently quarantined for
citrus canker.
We acknowledge that it is possible that all of these circumstances
could prevail, but such a ``perfect risk'' scenario would be an
extremely rare event. The commenter provides no evidence that could be
used to empirically estimate the frequency of this behavior, and APHIS
is unaware of any such evidence.
One commenter suggested a fruit-to-human-to-plant pathway for the
introduction of citrus canker into a commercial citrus-producing State.
A hobbyist who cultivates citrus in a State other than a commercial
citrus-producing State could handle infective citrus from the
quarantined area, then infect the plants the hobbyist is cultivating.
The hobbyist might not notice the canker infection and could
[[Page 65184]]
subsequently move the infected plants into a commercial citrus-
producing State.
We acknowledge that such an occurrence is possible, but such a
``perfect risk'' scenario would be an extremely rare event. The
commenter provides no evidence that could be used to empirically
estimate the frequency of such amateur citrus grower behavior, and
APHIS is unaware of any such evidence.
None of the pathway scenarios suggested by the commenters have
changed the RMA's conclusion that an unlikely sequence of
epidemiological events would have to occur for a successful Xac
infection that results in disease outbreaks to occur as a result of the
movement of commercially packed, treated, and APHIS-inspected fruit to
States other than commercial citrus-producing States.
Potential for Citrus Canker Establishment in Commercial Citrus-
Producing Areas
The RMA included a discussion of the susceptibility of commercial
citrus-producing areas that are not currently quarantined for citrus
canker to the spread of the disease. This discussion included a
reference to a study by Borchert et al. (2007) that developed a citrus
canker spread model using the North Carolina State University APHIS
Plant Pest Forecast System to identify areas where citrus canker could
become established in the major citrus-producing regions of the United
States.
Two commenters stated that modeling of pathogen establishment,
infection, and disease severity should be an essential component of the
risk assessment for each citrus-producing State and region within the
State, adding that the Borchert project results should be made publicly
available.
We disagree that modeling of pathogen establishment, infection, and
disease severity in commercial citrus-producing States is a necessary
component of the risk assessment. The RMA concluded that the
introduction and spread of Xac into other commercial citrus-producing
States through the movement of commercially packed fresh citrus fruit
from quarantined areas is unlikely. Nevertheless, because the RMA
concluded that the evidence is not currently sufficient to support a
determination that fresh citrus fruit produced in a Xac-infested grove
cannot serve as a pathway for the introduction of Xac into new areas,
we are prohibiting the interstate movement of fruit from a quarantined
area into commercial citrus-producing States. This measure makes
modeling of pathogen establishment, infection, and disease severity in
commercial citrus-producing States unnecessary.
The Borchert et al. (2007) study is an internal APHIS document. We
made the study available to commenters who requested it during the
comment period, and it is available from the person listed under FOR
FURTHER INFORMATION CONTACT. The Borchert et al. (2007) study provides
the modeling requested by the commenters.
Some commenters addressed the risk citrus canker posed to specific
States. One commenter stated that California is a fresh citrus State
with more than 200,000 acres dedicated to the fresh market production
of oranges, lemons, grapefruit, mandarins, and other citrus varieties.
Although the majority of the oranges are grown in arid areas, many of
the lemons and some of the grapefruit are produced in climates with
higher humidity and rainfall. The commenter stated that the survival of
canker in these areas would be expected; the survival of canker in the
more arid areas is less certain, but canker's potential impact cannot
be ignored based on survival reports from other arid lands. Another
commenter, addressing the suitability of California's climate for
development of citrus canker, stated that Dalla Pria et al. (2006)
stated that the greatest severity of canker occurred at 24 hours of
leaf wetness, with 4 hours of wetness being the minimum duration
sufficient to cause 100 percent incidence at optimal temperatures of 25
[deg]C to 35 [deg]C.
Another commenter stated that when Texas had citrus canker, it was
in southeast Texas, which has higher rainfall than the Rio Grande
Valley. The Rio Grande Valley generally has high relative humidity,
although the commenter stated that there is tremendous variability in
Texas' weather patterns; for example, July 2007 has been very wet. The
commenter stated that canker would be able to thrive in the conditions
present in the commercial growing area of South Texas. Surveys for
citrus greening, the commenter stated, have revealed that Texas has
substantial amounts of citrus in an area approximately 100 miles north
of the Gulf of Mexico from Brownsville to Houston. The commenter noted
that the challenges of eradicating canker in the urban areas of Florida
contributed to the failure of the eradication program and anticipated
that many of those same difficulties would be experienced in Texas if
citrus canker appeared in urban areas.
We agree with these commenters that citrus canker could be
introduced to California and Texas. The RMA cited Peltier and Frederich
(1926) as indicating that the disease ``could develop in all of the
citrus regions of the world sometime over the growing season.'' These
facts do not change our conclusions that (1) only a small portion of
each commercial citrus-producing State actually produces citrus, and an
even smaller portion has a climate suitable for canker disease
development; and (2) the climate in Florida is the most favorable of
any State for the development of citrus canker, and it would be more
difficult for citrus canker to be introduced into and subsequently
become established in any other State. Regardless, the remaining
uncertainty about the level of risk associated with the movement of
citrus fruit from a quarantined area has led us to maintain the current
prohibition on the movement of citrus fruit into commercial citrus-
producing States.
Two commenters urged APHIS to address the risk of spreading citrus
canker to other potential host areas, which may not be areas where
citrus is commercially produced. One commenter stated that citrus (not
just fruit-bearing trees) can be and is grown in other areas of the
United States, and those areas are also at risk of citrus canker. The
commenter noted that during the initial outbreak of citrus canker in
the mainland United States, disease outbreaks were also recorded in
Alabama, Mississippi, South Carolina, and Georgia. The commenter also
noted that Borchert et al. (2007) were tasked ``to identify areas where
citrus canker could become established in the major citrus producing
regions of the United States,'' rather than all the areas in the United
States in which citrus canker could become established.
These commenters recommended that the RMA and the proposed rule
take account not only of current commercial citrus-producing areas, but
also areas where citrus currently grows (even if it is not commercially
grown) and areas where citrus could grow, but does not currently. These
commenters stated that establishment of citrus canker in any such area
might subsequently lead to establishment in commercial areas, since
many of these areas are contiguous with commercial areas, and long-
distance transport now appears to be more likely than historically,
presumably due to the presence of the Asian leafminer (Phyllocnistis
citrella Stainton) in Florida. These commenters also stated that citrus
canker establishment in areas where citrus is not commercially produced
would lead to other pathways for establishment in areas where it is.
[[Page 65185]]
The focus of the citrus canker program has been on commercial
citrus-producing States because these States present the highest
likelihood for introduction of the disease, due to the density of
citrus plantings in those States. Prohibiting the movement of fruit
from areas quarantined for citrus canker to States other than
commercial citrus-producing States would be overly restrictive.
We acknowledge that dooryard plantings of citrus exist outside of
commercial citrus-producing States. However, while canker infection in
a State other than a commercial citrus-producing State could serve as a
pathway for introduction into a commercial citrus-producing State, as
discussed earlier under the heading ``Potential Pathways for Spread of
Citrus Canker Through Movement of Fruit,'' an unlikely sequence of
epidemiological events would have to occur in order for citrus canker
to be introduced and established through the movement of citrus fruit
from a quarantined area.
If, in the future, commercial quantities of citrus are planted in a
State that is not currently designated as a commercial citrus-producing
State, we will designate that State as a commercial citrus-producing
State in Sec. 301.75-5.
As discussed in the RMA, injuries caused by the Asian leafminer can
produce wounds that serve as infection courts in leaves and, to a
lesser extent, fruit, but the leafminer itself is not a vector for the
spread of citrus canker.
Potential Application of the Packinghouse-Based APHIS Inspection System
to Imported Citrus
The regulations in 7 CFR 319.28 prohibit the importation of citrus
fruit from areas where citrus canker is present, except for Unshu
oranges from Japan and Cheju Island, Republic of Korea, that are
produced in accordance with the systems approach described in paragraph
(b) of that section. The systems approach for Unshu oranges from Japan
and Korea requires measures to ensure that the oranges are produced in
an area free from citrus canker; for Unshu oranges from Japan, the
systems approach requirements also address the citrus fruit fly.
Several commenters expressed concern that the proposed regulations,
if implemented, could lead to requests from other citrus-producing
countries to export citrus fruit under conditions similar to those we
proposed for the interstate movement of fruit from citrus canker
quarantined areas. The commenters noted that, under international trade
agreements, APHIS has agreed not to impose conditions on the
importation of commodities that are more restrictive than those we
impose on the domestic movement of similar commodities. These
commenters stated that the RMA should consider the risk associated not
only with the interstate movement of citrus fruit from domestic
quarantined areas but also the risk associated with potential imports
from foreign citrus-producing areas affected with citrus canker.
One commenter who had expressed concern about illegal movement of
Florida citrus into commercial citrus-producing States stated that this
potential problem would only increase if citrus fruit was allowed to be
imported from foreign areas affected with citrus canker.
Our analysis of the risk associated with the importation of citrus
fruit from other countries where citrus canker exists under conditions
similar to those in this final rule would be conducted separately from
the analysis we conducted for this rulemaking. Before we would consider
using an approach similar to that promulgated in this final rule to
allow the importation of citrus fruit from canker-affected areas in
another country, the national plant protection organization of such a
country would need to submit a request that we do so. A country
requesting to be able to use this framework to export citrus to us
would have to demonstrate the ability to perform the required
treatments and phytosanitary inspections; it would also be required to
have a bilateral workplan in place with APHIS. Depending on the
circumstances, we may allow imports only through a preclearance program
staffed by APHIS inspectors whose salaries are funded by the exporting
country. In addition, there may be other citrus pests in foreign citrus
production areas whose risk would need to be mitigated separately from
the risk posed by citrus canker. For these reasons, we have not amended
the RMA that accompanies this final rule to discuss potential imports
from other countries.
One commenter specifically noted that the requirements for Unshu
oranges from Japan are not in harmony with the proposed rule.
The proposed rule and the risk management analysis are based on the
most recent science and our determination of the appropriate level of
protection for the citrus canker pathogen. We may reassess the risk
associated with the importation of Unshu oranges from Japan in the
future if Japan requests that we do so. If we reassess the risk
associated with Unshu oranges from Japan, as discussed earlier, the
assessment will take into account all relevant local conditions and all
pests that are present in Japanese citrus production areas.
It is important to note that Unshu oranges from Japan, if they are
fumigated for arthropod pests, are allowed to be imported into
commercial citrus-producing States, because they are produced under a
systems approach. Fruit moved interstate from citrus canker quarantined
areas is not allowed to be moved into those States under this final
rule.
One commenter noted that the term ``commercially packed'' can be
interpreted in different ways. In South Korea, the commenter stated,
one group of growers used a ``commercial'' packing shed that was no
more than 75 meters by 50 meters and in which the post-harvest
treatment with sodium hypochlorite was performed in a small bath. The
commenter stated that it is important to recognize that different
circumstances prevail in different countries when harmonizing domestic
regulations with import regulations.
We fully agree with the commenter that the circumstances in a
country would need to be assessed before we could allow the importation
of citrus from a citrus canker-affected area under conditions similar
to those under which we are allowing the movement of citrus from a
citrus canker quarantined area.
With regard to the specific circumstance cited by the commenter, we
have determined that it is necessary to define the term ``commercial
packinghouse'' in this final rule, given that the PRA and RMA analyzed
the risk associated with the interstate movement of commercially packed
fruit. In this final rule, we are adding a definition of commercial
packinghouse to the regulations. This definition reads: ``An
establishment in which space and equipment are maintained for the
primary purpose of packing citrus fruit for commercial sale. A
commercial packinghouse must be registered as a packinghouse with the
State in which it operates or hold a business license for treating and
packing fruit.'' This definition will help to ensure that the
packinghouses that pack fruit for interstate movement under this final
rule have equipment and operating procedures that are consistent with
those described in the PRA and RMA.
Because the PRA and RMA referred specifically to the risks
associated with commercially packed fruit, we are amending the proposed
regulations in Sec. 301.75-7 to refer specifically to commercial
packinghouses.
One commenter stated that implementation of the proposed rule
[[Page 65186]]
may also result in foreign countries requesting APHIS to consider a
similar approach for fresh commodities other than citrus. The commenter
stated that the approach described in the proposed rule could be
applied in any number of other situations in which a systems approach
is not operationally or financially feasible.
It is important to note in response to this comment that we
determine what phytosanitary mitigations are appropriate for the
importation or interstate movement of commodities based on our
assessment of the risk their importation or interstate movement poses
and the appropriate level of phytosanitary protection against that
risk. If we determined that a set of mitigations was necessary to
provide the appropriate level of protection for a commodity proposed
for importation, but that set of mitigations was determined not to be
operationally or financially feasible by the national plant protection
organization of the exporting country, we would not allow the
importation of that commodity.
We would only allow the importation of a commodity under an
approach similar to the approach used in this final rule if we
determined that this approach could provide the appropriate level of
phytosanitary protection. In past cases where we have determined that
inspection, treatment, and limited distribution mitigations similar to
those implemented in this final rule can provide an appropriate level
of protection against the introduction of plant pests by imported
commodities, we have employed such mitigations. For example, litchi
imported from Thailand are inspected for a fungal pathogen, irradiated
for arthropod pests, and prohibited from being imported or moved into
Florida due to the litchi rust mite.
In order for us to determine that a packinghouse-centered approach
provided an appropriate level of phytosanitary protection, we would
have to determine that the biology of the pest supported such an
approach and that the pest in question could be effectively detected by
inspection of the commodity. In addition, other considerations may
apply based on the level of risk we determine importation of the
commodity to pose.
Miscellaneous Comments on the RMA
One commenter noted that, since viable Xac have been found in
fruits with canker lesions that are imported into Europe, it is clear
that the importation of symptomless fruits from canker-infected areas
has a risk of introducing the disease if all the control steps, carried
out by many people at different times, are not always perfectly
implemented.
The RMA concluded that the introduction and spread of Xac into
other commercial citrus-producing States through the movement of
commercially packed fresh citrus fruit from quarantined areas is
unlikely. While fruit with visible canker lesions has likely been
imported into the EU, the importation of citrus fruit from areas where
citrus canker is present has not resulted in the introduction of the
disease in the EU, despite the fact that all fruit imported into the EU
is allowed to move to citrus-producing areas within the EU. (This is
discussed in more detail in the RMA in Section 5.6.2, ``International
and Interstate Movement of Citrus Fruit.'') In addition, treatment and
inspection will both serve as effective mitigations against the
potential of fruit moved interstate to introduce citrus canker to other
States. Nevertheless, the RMA concluded that the evidence is not
currently sufficient to support a determination that fresh citrus fruit
produced in a Xac-infested grove cannot serve as a pathway for the
introduction of Xac into new areas. That is why this final rule
prohibits the distribution of fruit moved interstate from quarantined
areas to commercial citrus-producing States.
In the RMA, we stated that there is no authenticated record of the
movement of fresh fruit infected with Xac being related to the
epidemiology of citrus canker disease. One commenter stated that pest-
free areas are now established on the basis of a pest being ``known (as
demonstrated by scientific evidence) not to occur'' rather than ``not
known to occur,'' and the same standard of evidence should apply to
this statement; research should be conducted to establish this
statement as fact.
We agree with the commenter's characterization of the process by
which pest-free areas are established. Our statement was not meant to
imply that we had positively established that fresh fruit infected with
Xac has never served as a pathway for the transmission of citrus
canker. Rather, it reflects the fact that no outbreaks of citrus canker
have ever been attributed to the movement of infected fruit, despite
the brisk global trade in such fruit. (The majority of outbreaks of
citrus canker whose cause is known were caused by the movement of
infected citrus nursery stock, rather than fruit.)
The RMA noted the Asian leafminer interacts with Xac by providing
wounds that serve as infection courts in leaves and, to a lesser
extent, fruit. Leafminer wounds create suitable microclimates for Xac
development, and leafminer-damaged leaves have more and larger lesions.
One commenter asked whether injuries from the peel miner, an insect
present in California, could result in higher infection of fruits.
Injuries from the peel miner would be likely to increase the
susceptibility of fruit to infection, and increase the severity of the
infection if they became infected. In terms of overall spread of citrus
canker, the peel miner would not likely be as epidemiologically
significant as the Asian leafminer, since leaves of citrus trees and
plants are more susceptible to citrus canker infection than the peels
of citrus fruit.
One section of the RMA discussed the effect of shipping and storage
temperatures on Xac populations, concluding that typical shipping and
storage temperatures reduce such populations. One commenter noted that
pathologists are able to keep Xac-infected samples in refrigerators at
2 [deg]C to 4 [deg]C and still isolate the bacterium. The commenter
stated that the emphasis of this section should be on the survival of
the bacterium.
We agree with the commenter that cool temperatures do not
necessarily cause mortality for Xac, and the RMA noted accordingly that
such temperatures influence survival rather than stating that they
inactivate the bacteria. However, in the context of an analysis of the
likelihood of citrus fruit serving as a pathway for the introduction or
spread of citrus canker, it is important to note that shipping and
storage temperatures reduce Xac populations. In addition, commercial
refrigeration is also quite dry, and Xac is highly influenced by
humidity, so the dryness of refrigeration is more likely to have
mortality effects than the cold.
The RMA stated that fruit are susceptible to citrus canker
infection from petal fall until they are around 6 cm in diameter, and
are most susceptible at a fruit diameter of about 2-4 cm. One commenter
stated that fruit size cannot be related to susceptibility unless the
variety is indicated, as some varieties (such as grapefruit) are bigger
than others (such as mandarins).
We agree with the commenter, and we have amended the discussion in
the RMA to state that fruit are susceptible to natural (stomatal)
infection from petal fall until they are fully expanded (around 6 cm in
diameter for some varieties), and are most susceptible after stomata
form and fruit is in a stage of rapid expansion, a period of about 90
to 120 days (at a fruit diameter of about 2-6 cm for some varieties).
In discussing the international and interstate movement of citrus
fruit, the
[[Page 65187]]
RMA noted that in 2004, India (where Xac is reported) shipped 8 metric
tons of citrus to Ghana and 2 metric tons to South Africa, and that no
outbreaks of Xac have been reported in any of the recipient countries.
One commenter stated that the shipment of citrus from India to South
Africa seems a dubious record.
These data were drawn from the Food and Agriculture Organization's
``World trade and crop production statistics'' database at http://
faostat.fao.org. The commenter provided no further information
establishing these records as dubious.
We also discussed the movement of fresh citrus from Florida during
Xac outbreaks. One commenter asked whether the earlier shipments of
Florida fruit were from canker-free areas, or at least canker-free
areas of production under official control.
We noted in the RMA that these shipments of Florida citrus may have
originated in areas of low prevalence or free of Xac. These shipments
were required to originate in groves that had been certified to be free
of Xac based on an inspection.
Comments on the Model in Appendix 1 to the RMA
As mentioned earlier, to assist in evaluating the options we
identified for packinghouse-centered risk management, we prepared a
quantitative model (Appendix 1 to the RMA) based on Florida production
and shipping data to evaluate the efficacy of three levels of
phytosanitary inspection in ensuring that fruit with visible canker
lesions does not enter commercial citrus-producing States. The three
inspection levels were determined by preliminary estimates of the Plant
Protection and Quarantine program's Citrus Health Response Program
staff of inspection levels that might be operationally feasible. The
three inspection levels evaluated were 500 fruit per lot, 1,000 fruit
per lot, and 2,000 fruit per lot. Statistically, randomized inspection
of 500, 1,000 fruit, or 2,000 fruit per lot will ensure, with 95
percent confidence, that the proportion of undetected fruit with
visible canker lesions in a cleared lot is no more than 0.75, 0.38, and
0.19 percent, respectively.
The outputs of the quantitative model were probability
distributions. The model determined, with 95 percent confidence, that
the total number of citrus fruit shipped from Florida to 5 citrus-
producing States (Arizona, California, Hawaii, Louisiana and Texas)
over a single shipping season would be 181,283,744 or less if unlimited
distribution is permitted. The model determined, with 95 percent
confidence, that the number of Xac-symptomatic fruit reaching those 5
States in a single shipping season would be 633,152 or less at the
1,000 randomly sampled fruit inspection level. We anticipate that about
double that number (approximately 1,266,304 or less) of Xac-symptomatic
fruit would reach those States at the 500 fruit inspectional level.
About half that number (approximately 316,576 or less) would reach
those States at the 2,000 fruit inspectional level. The model further
determined with 95 percent confidence that the number of symptomatic
fruit reaching citrus-producing areas within those States in a single
shipping season would be 2,135 or less at the 1,000 fruit inspectional
level, about double that number (approximately 4,270 or less) at the
500 fruit inspectional level, and about half that number (approximately
1,067 or less) at the 2,000 fruit inspectional level. (As discussed in
Section 9.3.3.4 of Appendix 1 to the RMA, the actual acreage on which
citrus is produced within a citrus-producing State is a small fraction
of the total acreage of that State.) The base level inspection of 1,000
randomly sampled fruit per lot was adopted because it is operationally
feasible with small adjustments to the current phytosanitary inspection
process in Florida.
The potential for fruit with visible canker lesions to reach
commercial citrus-producing States, coupled with the aforementioned
uncertainty regarding fruit as a pathway, led to the determination that
additional mitigations were required.
We received several comments from one commenter addressing the
model in Appendix 1 to the RMA.
The commenter stated that the model failed to take into account the
increased numbers of fruit that would be moved interstate from Florida
and imported from citrus canker-affected areas in other countries, and
thus underestimated the number of potentially infected fruit that could
reach commercial citrus-producing States. The commenter cited another
comment that estimated that the spread of canker has resulted in an
additional 20 percent of Florida's total fresh citrus groves becoming
ineligible for interstate movement under the regulations that were in
place before the publication of this final rule. That 20 percent, that
commenter stated, represents approximately 8 million 4/5-bushel cartons
or an approximately $80 million potential business opportunity under
the proposal.
The comment estimating the potential increase in fruit moved
interstate under this final rule is dealt with in more detail under the
heading ``Comments on the Preliminary Regulatory Impact Analysis and
Initial Regulatory Flexibility Analysis'' later in this document. We
have concluded that the increase in the number of fruit that will be
moved interstate under this final rule is likely much less than the
commenter estimates, although we have been unable to quantify the
probable increase.
This final rule does not change our requirements for the
importation of citrus fruit from areas in other countries where citrus
canker is present. Therefore, this final rule will not increase the
amount of fruit imported from such areas. As stated earlier in this
document under the heading ``Potential Application of the Packinghouse-
Based APHIS Inspection System to Imported Citrus,'' our analysis of the
risk associated with the importation of citrus fruit from other
countries where citrus canker exists under conditions similar to those
in this final rule would be conducted separately from the analysis we
conducted for the proposal and this final rule.
In Section 9.3.3.1 of Appendix 1, we determined probability
distributions for the number of \4/5\-bushel cartons shipped per
growing season for each commercial citrus-producing State destination
and variety of fruit. To determine the probability distributions, we
used the minimum, average, and maximum values of the last 4 years (2003
through 2006) of historical data on citrus fruit shipping from Florida
to other commercial citrus-producing States.
One commenter stated that the last 4 seasons of data have been
strongly affected by both natural events (damage caused by hurricanes,
tree destruction in an attempt to eradicate the canker outbreak) and
imposed movement restrictions (due to the canker outbreak). The
commenter noted that over the 10 years preceding the 2003 through 2006
data, the average domestic shipping quantity was 1.6 times higher than
it was during those years. The commenter stated that the uncertainty in
the expected average number of fruit that will be shipped from Florida
is therefore considerably higher than would be expected from
examination of just the last four seasons, unless APHIS considers that
the decline in numbers is a permanent feature of the Florida industry
and the last four seasons are typical.
The amount of citrus moved interstate has declined steadily since
the 1996-97
[[Page 65188]]
season, with a larger decline in 2004-05, when fruit production was
affected by hurricanes. (See figure 1.)
[GRAPHIC] [TIFF OMITTED] TR19NO07.000
The trends and changes occurring in the Florida citrus industry
suggest that the last four seasons are typical. The 2006 Commercial
Citrus Inventory for Florida (USDA-NASS 2007) states the following
about the 2-year trend for Florida citrus fruit production: ``Florida's
citrus acreage peaked again at 857,687 in 1996 but has been declining
ever since. The 2006 total is 621,373, down 17.0 percent in a 2-year
period noted for hurricanes, diseases, and urban development. The net
change, a loss of 127,182 acres, is the greatest in any non-freeze
period and 2nd overall. The Indian River District bore one-third of
this loss. Removals out-numbered new plantings by a ratio of more than
5:1. The 23,623 acres of new plantings are the least recorded in any
two-year period since 1970-71.'' The last two sentences are especially
germane to this discussion, as any rebound in Florida fresh citrus
production would depend on new plantings. The Commercial Citrus
Inventory also states that acreage decreases were reported for all 30
counties included in the survey, and that ``only 197,027 acres (28.2
percent) remain from the 697,929 reported in the 1988 census.'' This
evidence indicates a continued trend toward a decline in Florida citrus
production. Therefore, we are making no changes in response to this
comment. However, as shipping data for the 2006-07 season are now
available, we use those data in Appendix 1 of the RMA that accompanies
this final rule.
In Section 9.3.3.2 of Appendix 1 of the RMA, we presented a
determination of the number of fruit shipped per \4/5\-bushel carton.
We used USDA-National Agricultural Statistics Service (NASS) forecasts
of fruit sizes to determine percentage distributions for the number of
fruit that would be contained in each \4/5\-bushel carton, and then
used the minimum, mean, and maximum from each of these distributions as
parameters in a Pert distribution to define the number of fruit of each
variety per \4/5\-bushel carton.
The commenter made several comments about this technique, stating
that:
The USDA-NASS forecasts of fruit sizes are properly
represented by a discrete, rather than a continuous, distribution;
No basis was given for the use of Pert distributions to
account for the uncertainties in annual shipments;
The Pert distributions generated have mean values that
differ from the mean values of the data, because the mean values of the
data were improperly used as the modes for the Pert distributions;
The actual use of Pert distributions, which is
accomplished by fitting the discrete data to a Pert distribution and
then finding the mean and standard deviation of the Pert distribution,
is inefficient, not well defined, and has an unknown error rate; and
The Florida Department of Citrus has data on the actual
average numbers of fruit per \4/5\-bushel carton, which we should have
used.
The commenter stated that these flaws had an impact on a later
section of the analysis as well, Section 9.3.4, in which our evaluation
of the uncertainty associated with the number of fruit that will move
interstate from Florida relies on the uncertainty in the Pert
distributions that the commenter stated were incorrectly employed.
We agree that the analysis would have been improved by the use of
the actual average numbers of fruit per \4/5\-bushel carton. To improve
the model in Appendix 1 for this final rule, we have obtained from the
Florida Department of
[[Page 65189]]
Citrus the total number of \4/5\-bushel cartons of fruit for each type
and size of fruit that was shipped to commercial citrus-producing
States and the average number of fruit per bushel for each fruit size.
Our use of these data makes using the USDA-NASS fruit size forecasts
and the resulting Pert distributions unnecessary, thus addressing the
commenter's concerns.
For some varieties, using real data increases the numb